UV-C–Irradiated Arabidopsis and Tobacco Emit Volatiles That Trigger Genomic Instability in Neighboring Plants

Abstract

We have previously shown that local exposure of plants to stress results in a systemic increase in genome instability. Here, we show that UV-C–irradiated plants produce a volatile signal that triggers an increase in genome instability in neighboring nonirradiated Arabidopsis thaliana plants. This volatile signal is interspecific, as UV-C–irradiated Arabidopsis plants transmit genome destabilization to naive tobacco (Nicotiana tabacum) plants and vice versa. We report that plants exposed to the volatile hormones methyl salicylate (MeSA) or methyl jasmonate (MeJA) exhibit a similar level of genome destabilization as UV-C–irradiated plants. We also found that irradiated Arabidopsis plants produce MeSA and MeJA. The analysis of mutants impaired in the synthesis and/or response to salicylic acid (SA) and/or jasmonic acid showed that at least one other volatile compound besides MeSA and MeJA can communicate interplant genome instability. The NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 (npr1) mutant, defective in SA signaling, is impaired in both the production and the perception of the volatile signals, demonstrating a key role for NPR1 as a central regulator of genome stability. Finally, various forms of stress resulting in the formation of necrotic lesions also generate a volatile signal that leads to genomic instability.

Reevaluation of the Reliability and Usefulness of the Somatic Homologous Recombination Reporter Lines

“…The data obtained mostly from the somatic homologous recombination (SHR) reporter lines suggests that repair of such damage seems to increase the frequency not only of meiotic but also SHR events (reviewed in Boyko and Kovalchuk, 2011;Waterworth et al, 2011). A number of research articles in this area suggest that increases in homologous recombination (HR) frequencies may be a programmed response to accelerate evolutionary adaption and generate new resistance traits, enabling greater genomic plasticity in plants in response to adverse environmental conditions (Molinier et al, 2006;Boyko and Kovalchuk, 2011;Yao et al, 2011). However, we question the validity of these conclusions since these data are obtained almost exclusively using the SHR reporter lines that are not adequately characterized in the published literature.…”

“…Stress (UV-C or flagellin) applied to Arabidopsis plants increased levels of HR that persisted in several subsequent, untreated generations (Molinier et al, 2006). Most recently, it was shown that volatile signals from stressed plants also trigger an increase in genome instability in neighboring unstressed plants (Yao et al, 2011).…”

“…This scenario is also possible for hybrid polypeptides originating from a plant gene and LUC/GUS transgene. Since in some publications, such as Yao et al (2011), neither the sequence of the linker DNA nor the plant locus where the transgene is located is given, we cannot determine whether these DNA sequences might act as inteins in reconstitution of functional LUC/GUS enzymes upon transcription and translation.…”

“…Therefore, analysis of several different lines is necessary to get the most reliable data. For example, Yao et al (2011) used only one line (line 15D8) for their analysis. This is understandable for the crosses with the Arabidopsis hormone signaling mutants.…”

“…In most cases the information about these linker DNA sequences is missing, incomplete, or possibly inaccurate. For example, Yao et al (2011) reported that they employed a 500 bp noncoding DNA fragment as linker. However, after consulting the references cited, we found that the linker sequence used in their study in fact appears to be much larger and contains the bar gene cassette providing resistance to phosphinothricin (Gorbunova et al, 2000).…”